Secreted nucleases reclaim extracellular DNA during biofilm development.

IF 7.8 1区生物学 Q1 BIOTECHNOLOGY & APPLIED MICROBIOLOGY

npj Biofilms and Microbiomes Pub Date : 2024-10-07 DOI:10.1038/s41522-024-00575-9

Stephen M Lander, Garth Fisher, Blake A Everett, Peter Tran, Arthur Prindle

{"title":"Secreted nucleases reclaim extracellular DNA during biofilm development.","authors":"Stephen M Lander, Garth Fisher, Blake A Everett, Peter Tran, Arthur Prindle","doi":"10.1038/s41522-024-00575-9","DOIUrl":null,"url":null,"abstract":"DNA is the genetic code found inside all living cells and its molecular stability can also be utilized outside the cell. While extracellular DNA (eDNA) has been identified as a structural polymer in bacterial biofilms, whether it persists stably throughout development remains unclear. Here, we report that eDNA is temporarily invested in the biofilm matrix before being reclaimed later in development. Specifically, by imaging eDNA dynamics within undomesticated Bacillus subtilis biofilms, we found eDNA is produced during biofilm establishment before being globally degraded in a spatiotemporally coordinated pulse. We identified YhcR, a secreted Ca2+-dependent nuclease, as responsible for eDNA degradation in pellicle biofilms. YhcR cooperates with two other nucleases, NucA and NucB, to reclaim eDNA for its phosphate content in colony biofilms. Our results identify extracellular nucleases that are crucial for eDNA reclamation during biofilm development and we therefore propose a new role for eDNA as a dynamic metabolic reservoir.","PeriodicalId":19370,"journal":{"name":"npj Biofilms and Microbiomes","volume":"10 1","pages":"103"},"PeriodicalIF":7.8000,"publicationDate":"2024-10-07","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11458576/pdf/","citationCount":"0","resultStr":null,"platform":"Semanticscholar","paperid":null,"PeriodicalName":"npj Biofilms and Microbiomes","FirstCategoryId":"99","ListUrlMain":"https://doi.org/10.1038/s41522-024-00575-9","RegionNum":1,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":null,"EPubDate":"","PubModel":"","JCR":"Q1","JCRName":"BIOTECHNOLOGY & APPLIED MICROBIOLOGY","Score":null,"Total":0}

引用次数: 0

Abstract

DNA is the genetic code found inside all living cells and its molecular stability can also be utilized outside the cell. While extracellular DNA (eDNA) has been identified as a structural polymer in bacterial biofilms, whether it persists stably throughout development remains unclear. Here, we report that eDNA is temporarily invested in the biofilm matrix before being reclaimed later in development. Specifically, by imaging eDNA dynamics within undomesticated Bacillus subtilis biofilms, we found eDNA is produced during biofilm establishment before being globally degraded in a spatiotemporally coordinated pulse. We identified YhcR, a secreted Ca²⁺-dependent nuclease, as responsible for eDNA degradation in pellicle biofilms. YhcR cooperates with two other nucleases, NucA and NucB, to reclaim eDNA for its phosphate content in colony biofilms. Our results identify extracellular nucleases that are crucial for eDNA reclamation during biofilm development and we therefore propose a new role for eDNA as a dynamic metabolic reservoir.

查看原文本刊更多论文

分泌的核酸酶在生物膜发育过程中回收细胞外 DNA。

DNA 是所有活细胞内的遗传密码，其分子稳定性也可用于细胞外。虽然细胞外 DNA（eDNA）已被确认为细菌生物膜中的一种结构聚合物，但它是否会在整个发育过程中稳定存在仍不清楚。在此，我们报告了 eDNA 在生物膜基质中的临时投入，然后在发育后期被回收。具体来说，通过对未驯化枯草芽孢杆菌生物膜内的 eDNA 动态成像，我们发现 eDNA 在生物膜建立过程中产生，然后以时空协调的脉冲方式被全面降解。我们发现 YhcR 是一种分泌型 Ca2+ 依赖性核酸酶，负责胶粒生物膜中 eDNA 的降解。YhcR 与另外两种核酸酶 NucA 和 NucB 合作，在菌落生物膜中回收 eDNA 的磷酸盐含量。我们的研究结果确定了在生物膜发育过程中对 eDNA 回收至关重要的细胞外核酸酶，因此我们提出了 eDNA 作为动态代谢库的新作用。

本文章由计算机程序翻译，如有差异，请以英文原文为准。

求助全文

约1分钟内获得全文求助全文

来源期刊

npj Biofilms and Microbiomes Immunology and Microbiology-Microbiology

CiteScore

12.10

自引率

3.30%

发文量

审稿时长

9 weeks

期刊介绍： npj Biofilms and Microbiomes is a comprehensive platform that promotes research on biofilms and microbiomes across various scientific disciplines. The journal facilitates cross-disciplinary discussions to enhance our understanding of the biology, ecology, and communal functions of biofilms, populations, and communities. It also focuses on applications in the medical, environmental, and engineering domains. The scope of the journal encompasses all aspects of the field, ranging from cell-cell communication and single cell interactions to the microbiomes of humans, animals, plants, and natural and built environments. The journal also welcomes research on the virome, phageome, mycome, and fungome. It publishes both applied science and theoretical work. As an open access and interdisciplinary journal, its primary goal is to publish significant scientific advancements in microbial biofilms and microbiomes. The journal enables discussions that span multiple disciplines and contributes to our understanding of the social behavior of microbial biofilm populations and communities, and their impact on life, human health, and the environment.